Evolution of DNA Polymerase Families: Evidences for Multiple Gene Exchange Between Cellular and Viral Proteins

Filée, Jonathan; Forterre, Patrick; Tang, Sen‐Lin; Laurent, Jacqueline

doi:10.1007/s00239-001-0078-x

Cited by 225 publications

(219 citation statements)

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“…A maximum likelihood tree encompassing all the polymerase groups described in (Filee et al, 2002) and trimmed to their specified conserved regions confirmed that metagenomic Clade I-III are not related to the group of phages encoding DNA pol g-like polymerases (Supplementary Figure S5). The clades containing metagenomic representative sequences described in Figure 1 remained distinct and did not disrupt previously established relationships, further supporting our finding that these clades are valid groupings linked to polymerase functionality.…”

Section: Discussionmentioning

confidence: 87%

Shotgun metagenomics indicates novel family A DNA polymerases predominate within marine virioplankton

et al. 2013

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Virioplankton have a significant role in marine ecosystems, yet we know little of the predominant biological characteristics of aquatic viruses that influence the flow of nutrients and energy through microbial communities. Family A DNA polymerases, critical to DNA replication and repair in prokaryotes, are found in many tailed bacteriophages. The essential role of DNA polymerase in viral replication makes it a useful target for connecting viral diversity with an important biological feature of viruses. Capturing the full diversity of this polymorphic gene by targeted approaches has been difficult; thus, full-length DNA polymerase genes were assembled out of virioplankton shotgun metagenomic sequence libraries (viromes). Within the viromes novel DNA polymerases were common and found in both double-stranded (ds) DNA and single-stranded (ss) DNA libraries. Finding DNA polymerase genes in ssDNA viral libraries was unexpected, as no such genes have been previously reported from ssDNA phage. Surprisingly, the most common virioplankton DNA polymerases were related to a siphovirus infecting an a-proteobacterial symbiont of a marine sponge and not the podoviral T7-like polymerases seen in many other studies. Amino acids predictive of catalytic efficiency and fidelity linked perfectly to the environmental clades, indicating that most DNA polymerase-carrying virioplankton utilize a lower efficiency, higher fidelity enzyme. Comparisons with previously reported, PCR-amplified DNA polymerase sequences indicated that the most common virioplankton metagenomic DNA polymerases formed a new group that included siphoviruses. These data indicate that slower-replicating, lytic or lysogenic phage populations rather than fast-replicating, highly lytic phages may predominate within the virioplankton.

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Section: Discussionmentioning

confidence: 87%

Shotgun metagenomics indicates novel family A DNA polymerases predominate within marine virioplankton

et al. 2013

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“…Indeed, the overall picture becomes more complex when proteins involved in DNA replication, recombination, or repair (DNA informational proteins) are taken into account. The reason is that many DNA informational proteins do not display the classical pattern, i.e., three homologous versions (one for each domain) (18)(19)(20)(21)(22). In particular, the major proteins involved in bacterial DNA replication (DNA polymerase, primase, and helicase) are not homologous to their archaeal͞eukaryal counterparts (i.e., there is only one version of the DnaG primase, the bacterial one, and two versions of the archaeal͞eukaryal primase).…”

Section: The Multiple Versions and Erratic Distribution Of Dna Informmentioning

confidence: 99%

Three RNA cells for ribosomal lineages and three DNA viruses to replicate their genomes: A hypothesis for the origin of cellular domain

Forterre

2006

Proc. Natl. Acad. Sci. U.S.A.

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The division of the living world into three cellular domains, Archaea, Bacteria, and Eukarya, is now generally accepted. However, there is no consensus about the evolutionary relationships among these domains, because all of the proposed models have a number of more or less severe pitfalls. Another drawback of current models for the universal tree of life is the exclusion of viruses, otherwise a major component of the biosphere. Recently, it was suggested that the transition from RNA to DNA genomes occurred in the viral world, and that cellular DNA and its replication machineries originated via transfers from DNA viruses to RNA cells. Here, I explore the possibility that three such independent transfers were at the origin of Archaea, Bacteria, and Eukarya, respectively. The reduction of evolutionary rates following the transition from RNA to DNA genomes would have stabilized the three canonical versions of proteins involved in translation, whereas the existence of three different founder DNA viruses explains why each domain has its specific DNA replication apparatus. In that model, plasmids can be viewed as transitional forms between DNA viruses and cellular chromosomes, and the formation of different levels of cellular organization (prokaryote or eukaryote) could be traced back to the nature of the founder DNA viruses and RNA cells.

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“…The majority of identified DNA polymerases can be classified into Families A, B, C, and Y according to amino acid sequence similarities to Escherichia coli polymerases I, II, III, and IV/V, respectively (4,5). Additional families have been identified, including the two-subunit replicative DNA polymerases from hyperthermophilic Archaea (Family D) (6) and eukaryotic DNA polymerase ␤ and terminal transferases (Family X) (4).…”

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confidence: 99%

Comparative Kinetics of Nucleotide Analog Incorporation by Vent DNA Polymerase

Gardner

Joyce

Jack

2004

Journal of Biological Chemistry

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Comparative kinetic and structural analyses of a variety of polymerases have revealed both common and divergent elements of nucleotide discrimination. Although the parameters for dNTP incorporation by the hyperthermophilic archaeal Family B Vent DNA polymerase are similar to those previously derived for Family A and B DNA polymerases, parameters for analog incorporation reveal alternative strategies for discrimination by this enzyme. Discrimination against ribonucleotides was characterized by a decrease in the affinity of NTP binding and a lower rate of phosphoryl transfer, whereas discrimination against ddNTPs was almost exclusively due to a slower rate of phosphodiester bond formation. Unlike Family A DNA polymerases, incorporation of 9-[(2-hydroxyethoxy)methyl]X triphosphates (where X is adenine, cytosine, guanine, or thymine; acyNTPs) by Vent DNA polymerase was enhanced over ddNTPs via a 50-fold increase in phosphoryl transfer rate. Furthermore, a mutant with increased propensity for nucleotide analog incorporation (Vent A488L DNA polymerase) had unaltered dNTP incorporation while displaying enhanced nucleotide analog binding affinity and rates of phosphoryl transfer. Based on kinetic data and available structural information from other DNA polymerases, we propose active site models for dNTP, ddNTP, and acyNTP selection by hyperthermophilic archaeal DNA polymerases to rationalize structural and functional differences between polymerases.All free living organisms encode several DNA polymerases that are jointly responsible for the replication and maintenance of their genomes, thereby ensuring accurate transmission of genetic information (1-3). The majority of identified DNA polymerases can be classified into Families A, B, C, and Y according to amino acid sequence similarities to Escherichia coli polymerases I, II, III, and IV/V, respectively (4, 5). Additional families have been identified, including the two-subunit replicative DNA polymerases from hyperthermophilic Archaea (Family D) (6) and eukaryotic DNA polymerase ␤ and terminal transferases (Family X) (4).Structural and kinetic analyses of Family A (7-14) and Family B (15-25) DNA polymerases have increased the understanding of nucleotide selection and incorporation mechanisms. Although amino acid sequences diverge between these two families, the structures of Family A and B DNA polymerases share recognizable finger, thumb, and palm subdomains that allow comparison of structural elements important for function (3, 11). In the case of Family A DNA polymerases from bacteriophage T7, Escherichia coli (Klenow fragment, large fragment of DNA polymerase I), and Thermus aquaticus, as well as the Family B DNA polymerase from bacteriophage RB69, interpretation of the structural information is complemented by steady-state and pre-steady-state kinetic studies, allowing a detailed description of the polymerization pathway. Reaction parameters describing the discrimination against naturally occurring nucleotide analogs encountered in vivo, such as NTPs, or unnatural n...

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Evolution of DNA Polymerase Families: Evidences for Multiple Gene Exchange Between Cellular and Viral Proteins

Cited by 225 publications

References 37 publications

Shotgun metagenomics indicates novel family A DNA polymerases predominate within marine virioplankton

Shotgun metagenomics indicates novel family A DNA polymerases predominate within marine virioplankton

Three RNA cells for ribosomal lineages and three DNA viruses to replicate their genomes: A hypothesis for the origin of cellular domain

Comparative Kinetics of Nucleotide Analog Incorporation by Vent DNA Polymerase

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